Population-parameter sensing in the mating system of Saccharomyces cerevisiae

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Abstract

Sexual reproduction is a key evolutionary innovation which sets the ground for sexual selection. Sexual selection exhibits a strong dependence on the degree of competition in a mating population. The tie between active perception of competition and sexual behavior is a crucial process for intra and intersexual selection, however, its mechanisms remain largely unknown due to experimental intractability. Unicellular mating occurs under the same constraints but population and environmental parameters can be experimentally controlled and dynamic measurements of molecular and behavioral outputs can be performed. In this work, we propose that on the prototypical chemosensory mating system from Saccharomyces cerevisiae, the response magnitude generated by the presence of the complementary sex equals the probability of forming a sexual pair by chance. In chemosensory (pheromonal) mating systems, perception of competition as an indicator of mating likelihood is constrained by the following fact. Given that the most reasonable measure of the degree of competition/mating-likelihood in the population is the operational sex ratio, i.e. the fraction of individuals of a particular sex in the sexually active population (OSR in animals or theta in this work), sensory systems would need information about the abundance of individuals of both sexes, whereas the sexual response is induced by pheromones produced only by the opposite sex. Therefore, the OSR seems sensorially indistinguishable from the absolute number of potential mates, which would make mating likelihood imperceptible. By using experiments where the emitted pheromone concentration is isotropic and therefore does not depend on the distance separating mates, we manipulated population parameters and measured quantitative mating-pheromone pathway outputs to show that yeast is able to effectively sense the population sex ratio (theta) and the absolute mate number as separate cues by using a sensory disentangling mechanism. The mechanism is based on sensory input attenuation, i.e. the enzymatic degradation of the sexual pheromone produced by the opposite sex. As revealed by a simple physical model, the population displays specific sensitivities to sex ratio and cell density by modifying the time profile of pheromone concentration, with its maxima depending linearly on emitter cell density, and scaled by the inverse square root of receiver cell density. We show that in a random collision scenario the sex-ratio of the population indeed determines the likelihood of successful sexual pairing, matching the gene-expression response to sex ratio. Sensing mating likelihood allows control of mating investments, minimizing growth arrest and pathway overstimulation. Pheromone-based mate-sensing constitutes an example of a population-level fractional sensing mechanism, aided by the coupling of population-dependent signal attenuation and internal non-adaptive signal transduction. The study can be framed within the context of quantitative biology in its experimental methodology, and within (cellular) sensory systems, cell-cell communication and sexual selection theory because of its implications.